Surveillance of listeriosis in the Tel Aviv District, Israel, 2010-2015
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Epidemiology and Infection Surveillance of listeriosis in the Tel Aviv District,
cambridge.org/hyg
Israel, 2010–2015
M. Salama1, Z. Amitai1, A. V. Ezernitchi2, R. Sheffer1, J. Jaffe2, S. Rahmani1,
E. Leshem3 and L. Valinsky2
Original Papers
1
Tel Aviv District Health Office, Ministry of Health, Tel Aviv, Israel; 2Central Laboratories, Israel Ministry of Health,
Cite this article: Salama M, Amitai Z, POB 34410, Jerusalem, 94467, Israel and 3Infectious Diseases Unit, The Chaim Sheba Medical Center, Tel Hashomer,
Ezernitchi AV, Sheffer R, Jaffe J, Rahmani S,
Israel
Leshem E, Valinsky L (2018). Surveillance of
listeriosis in the Tel Aviv District, Israel, 2010–
2015. Epidemiology and Infection 146, 283–290. Abstract
https://doi.org/10.1017/S0950268817003004
This study analyses the epidemiologic, clinical and molecular findings of all culture-confirmed
Received: 25 June 2017 cases of listeriosis notified from 2010 to 2015 in the Tel Aviv District, which is known to have
Revised: 29 November 2017 high rates of listeriosis. All clinical isolates of Listeria monocytogenes were subtyped using two-
Accepted: 30 November 2017 enzyme pulsed-field gel electrophoresis. During the studied period, 102 cases of listeriosis
First published online: 8 January 2018
were notified, including 23 pregnancy-associated cases (23%). Among 79 non-pregnancy-
Key words: associated cases, 18 had neuro-invasive disease (21%). There were 26 deaths associated with
Listeria; food-borne infections the disease. Using molecular identification, we found a number of clusters of identical bacter-
ial clones, which pointed to possible sources of infection. The high rates of morbidity and
Author for correspondence:
Matanelle Salama, E-mail: Matanelle.salama@
mortality resulting from listeriosis, as well as the diverse ways of infection demonstrated in
gmail.com this study, accentuate the need to boost public health actions, in order to raise awareness
and better control high-risk contamination routes.
Introduction
Listeria monocytogenes is a Gram-positive facultative anaerobic bacterium. Although L. mono-
cytogenes is ubiquitous and commonly found in the environment, humans get infected mostly
through ingestion of contaminated food.
Human infection with L. monocytogenes, listeriosis, is a rare disease which may be severe
and even fatal in at-risk populations. Symptoms of listeriosis appear to be host-dependent and
can range from a mild self-resolving gastro-intestinal illness to an invasive form of the disease,
which can cause bacteraemia and meningitis. Persons particularly at risk for invasive disease
include pregnant women, elderly and immunosuppressed individuals, with an overall case
fatality rate of 20–30% [1, 2]. Among infected pregnant women, bacteria may cross the pla-
centa and infect the foetus, leading to premature birth, abortion or neonatal listeriosis.
L. monocytogenes is classified in four lineages (I, II, III and IV) and 13 serotypes. The most
common circulating strains are from lineage I (serotype 4b and 1/2b) and lineage II (serotype
1/2a and 1/2c) [3]. The bacterium is salt tolerant and can grow at a wide range of pH and at
extreme temperatures (ranging from −0.4 to 45 °C [4]), which are significant advantages for its
survival and persistence in the environment and hence, its ability to contaminate.
Listeriosis has been a notifiable disease, by clinicians as well as laboratories, in Israel since
1996 [5]. All cases are notified to the relevant district office and the L. monocytogenes isolates
are sent to the National Reference Laboratory for confirmation and subtyping. Surveillance has
shown that its national incidence in Israel varies from 0.2 to 0.8/100 000 population per year
[6]. The rate of pregnancy-associated listeriosis in Israel was found to be among the highest
worldwide with up to 25.2 cases per 100 000 live births [4].
Listeriosis rates in the Tel Aviv District were observed to be higher compared to overall
national rates [7].
We report epidemiologic, clinical and molecular findings of listeriosis to further under-
stand the high rates of morbidity and exposure.
Materials and methods
A case of listeriosis was defined as a patient from whom L. monocytogenes was isolated from a
normally sterile site (e.g., blood or cerebrospinal fluid or, less commonly, joint, pleural or peri-
cardial fluid). Pregnancy-associated cases were defined as cases with a L. monocytogenes iso-
© Cambridge University Press 2018 lation from a pregnant woman, her foetus, or from a newborn up to 1-month old. A mother–
neonate pair was defined as a pair for which L. monocytogenes was isolated from both the
mother and the neonate. The study only included residents of the Tel Aviv District.
Each case of culture-confirmed listeriosis is notified to the Tel Aviv District Health Office.
A trained nurse contacts the patient or a close relative and initiates an epidemiologic
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https://doi.org/10.1017/S0950268817003004
284 M. Salama et al.
investigation. A structured questionnaire [8] is used to clarify the endonucleases, XbaI and AvrII, in two separate experiments [9].
disease presentation, underlying medical conditions and food PFGE patterns were analysed by the BioNumerics software
consumptions up to 2 months preceding disease onset. The ques- (Applied Maths) followed by unweighted pair group method
tionnaire includes a list of popular foods that were recalled in with arithmetic mean clustering analysis. Clones were assigned
Israel for L. monocytogenes contamination such as hummus, a number according to the international PulseNet criteria.
raw, smoked and cured fish, deli meat and dairy products. The
list is passed thereafter to the District Food Service for food sam-
pling in the retail stores where the food was purchased by the Statistical analysis
patient. In the case of packaged food, samples are taken from All the data collected were evaluated using IBM SPSS Statistics
sealed packages only. Restaurants in which cases consumed 23.0 Armonk, NY: IBM Corp. Given our relatively small sample,
food during the 2 months preceding illness onset undergo sani- analysis of continuous variables was done using Kruskal–Wallis H
tary inspections and relevant food samples are taken. According test, and categorical variables with a χ 2 test. A two-tailed value of
to the results of the inspection and/or if positive food samples P inferior or equal to 0.05 was considered statistically significant.
are identified, the restaurant, retail store or food factory undergo
corrective measures, repeated inspections and the district phys-
ician is informed. Additionally, the Israeli food safety legislation Results
requires food factories and restaurants to undergo routine inves- Epidemiologic characteristics
tigations and sampling, as it is mandatory to provide food free
of L. monocytogenes. During the years 2010–2015, 102 cases of culture-confirmed lis-
Clinical and socio-demographic data regarding patients were teriosis were notified to the Tel Aviv District Health Office. All
collected from hospital files. Patients were classified as having cases were hospitalised. Among them, 69 (68%) cases were
either neuro-invasive disease (NID) which included meningitis, women. Of all cases, 23 (23%) cases were pregnancy associated.
encephalitis or meningo-encephalitis, blood stream infection There were 26 (25%) deaths associated with the illness.
(BSI) or infection in another bodily site with L. monocytogenes. During the studied years, rates of listeriosis in the Tel Aviv
Deaths that occurred within 1 month of diagnosis were consid- District were grossly twice as high as the overall national rates
ered as illness associated. Hospital-acquired disease was defined (0.8–1.8/100 000 vs. 0.4–0.9/100 000 population per year).
as a case for which exposure to food, during the entire 2 months Compared to the other Israeli districts, rates of listeriosis were
prior to disease onset, was in a hospital or a nursing home. consistently higher in the Tel Aviv District (Fig. 1).
Possible hospital-acquired infection was defined as a case having Age-specific disease rates in the Tel Aviv District were also
been exposed to food anytime in the 2 months prior to disease higher in all age categories compared to national rates (Fig. 2).
onset in a hospital or nursing home. We did not find a seasonal trend in illness onset in the Tel
Aviv District but we did find that disease peaked in May and
September, in which two major Jewish holidays (the Jewish
Laboratory analysis New Year and the Israeli Independence Day) occur (Fig. 3).
Each isolate of L. monocytogenes identified by the diagnostic
laboratory is sent to the National Listeria Reference Laboratory Non-pregnancy-associated cases
for confirmation and serotype identification. Serotyping was per- Among 79 notified cases, median age was 76 years old (range 4–
formed with commercial antisera (Denka Seiken, Tokyo, Japan). 100). There were 31 men (39%) and 48 women (61%). Seven cases
Since 2007 L. monocytogenes from all clinical cases and most were nursing home residents. Fifteen patients (19% of cases) had
of the positive food samples are subtyped by pulse field gel elec- possible or proven hospital acquisition.
trophoresis (PFGE). The PulseNet standardised PFGE protocol Median duration of hospitalisation was 10 days (range 1–54).
for L. monocytogenes was performed with two restriction Seven cases (9%) were hospitalised in the intensive care unit,
Fig. 1. Rates of listeriosis per 100 000 population in the
different districts in Israel, 2010–2015.
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https://doi.org/10.1017/S0950268817003004
Epidemiology and Infection 285
Fig. 2. Age-specific listeriosis rates in the Tel Aviv Districts
and national age-specific listeriosis rates, 2010–2015.
two of which required mechanical ventilation. All patients had at included deli meats, hummus and sushi. Ten women reported
least one underlying medical condition (Table 1). Eighteen cases having eaten in various restaurants.
(23%) had NID, 54 (68%) had BSI. Three patients had L. mono- Among pregnant women, mean age was 31 years old (range
cytogenes infection in an isolated body site (one patient with 19–40). Pregnancy outcomes included seven (30%) miscarriages,
wound infection, one with arthritis and one with peritonitis). five (22%) pre-term births, five (22%) cases of neonatal listeriosis
The occurrence of NID was not significantly associated with and six (26%) normal ongoing pregnancies.
age, gender or L. monocytogenes serotype. Mean duration of hos- We found a statistically significant association between trimes-
pitalisation was significantly longer for patients with NID com- ter of pregnancy in which disease was diagnosed and pregnancy
pared with patients with BSI (Table 2). outcome. There were significantly more cases of neonatal listeri-
All 26 deaths observed in this study were non-pregnancy asso- osis and pre-term births when disease was diagnosed in the
ciated (case fatality rate in this category was 33%). There was no third trimester, and more miscarriages when diagnosed in the
significant association between death occurrence and L. monocy- first or second trimester (P = 0.012) (Table 3).
togenes serotype or clinical presentation (P > 0.05).
The most common food histories included consumption of
pre-packed commercial hummus (23%), cured or smoked fish
(20%), deli meats (17%) and sausages (9%). Seven patients (9%) Laboratory results
reported having eaten in restaurants during the 2 months prior The bacterial serotype was identified for 84 isolates. Fifty-two per
to their illness onset. cent were serotype 4b, 25% were serotype 1/2a and 23% were sero-
type 1/2b (Fig. 4). All three subtypes were isolated among
Pregnancy-associated cases non-pregnancy-associated cases, but among pregnancy-associated
Twenty-three pregnancy-associated cases were observed in this cases bacterial isolates solely belonged to lineage I (serotypes 4b
study, approximately 15 cases per 100 000 live births in the Tel and 1/2b). There was no statistically significant association
Aviv District. Seventeen (74%) were pregnant women and six between bacterial serotype and number of deaths or duration of
(26%) were newborns. Among them, there were three identified hospitalisation. Moreover, there was no significant association
mother–neonate pairs. Their most common food consumptions between serotype and pregnancy outcome (P > 0.05).
Fig. 3. Monthly distribution of the number of cases of
listeriosis during the years, Tel Aviv District, Israel,
2010–2015.
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https://doi.org/10.1017/S0950268817003004286 M. Salama et al.
Table 1. Demographic and clinical characteristics of non-pregnancy-associated and was discharged in good condition. The second case was born
listeriosis cases, Tel Aviv District, Israel, 2010–2015 spontaneously to an asymptomatic mother at 39 weeks GA, was
Alive (%) Dead (%) Total (%) discharged home and was readmitted a week post-discharge
with NID. The mothers did not report common exposures and
Total 53 26 79 did not live in the same city. The identical L. monocytogenes geno-
Age categories
type was isolated in raw fish in that same year. However, the
women did not report having eaten fish during their pregnancy.
80 14 (26.4%) 15 (26.4%) 29 (36.7%) Clusters 2 and 5 included both pregnancy and non-pregnancy-
Gender associated cases. In both clusters, the same L. monocytogenes pul-
Male 20 (37.7%) 11 (42.3%) 31 (39.2%)
sotype was not isolated from any food source.
Cluster 2 involved three cases living a few blocks apart in the
Female 33 (62.3%) 15 (57.7%) 48 (60.8%) same city, two of which fell ill 1 month apart. The third was diag-
Underlying medical nosed 3 years later. The two non-pregnancy-associated cases died
conditions as a result of the disease and no food histories were collected. The
Haematologic 10 (18.9%) 2 (7.7%) 12 (15.2%) pregnancy-associated case reported having consumed deli meats
malignancy as well as frozen fish at home and uncooked salads at a restaurant,
Solid tumour (in situ 20 (37.7%) 12 (46.2%) 32 (40.5%)
which underwent a sanitary investigation during which salads
or metastatic) were found to be kept above the recommended temperatures
but samples were negative for the presence of L. monocytogenes.
Inflammatory bowel 4 (7.5%) 1 (3.8%) 5 (6.3%)
disease
In cluster 5, most cases were pregnancy-associated (six out of
eight cases). Pregnancy outcomes included one normal ongoing
Diabetes mellitus 13 (24.5%) 5 (19.2%) 18 (22.8%) pregnancy and five abnormal outcomes (two pre-term births,
Hypertension 28 (52.8%) 16 (61.5%) 44 (55.7%) two cases of neonatal listeriosis and one miscarriage). Five out
Chronic renal failure 6 (11.3%) 6 (23.1%) 12 (15.2%)
of eight patients reported having eaten in various restaurants in
Tel Aviv, but all food samples taken were negative for listeria.
Heart disease 8 (15.1%) 11 (42.3%) 19 (24.1%) Cluster 3 included seven cases, one of which was pregnancy-
Immunosuppressive associated. Two cases had NID, the remainder had BSI. Among
treatment non-pregnancy-associated cases, all patients were older than 60
Corticosteroids 12 (22.6%) 4 (15.4%) 16 (20.3%) years (mean age was 77.67) and had underlying medical condi-
tions. Two patients died during hospitalisation. All five cases
Chemotherapy 9 (17%) 7 (26.9%) 16 (20.3%)
for which data on food consumption were available reported hav-
Immunomodulators 5 (9.4%) 1 (3.8%) 6 (7.6%) ing eaten a popular brand of pre-packed deli meat. Incidentally,
Disease presentation the identical L. monocytogenes pulsotype had been isolated from
that same brand of pre-packed deli meat during routine sampling.
Neuro-invasive 14 (26.4%) 4 (15.4%) 18 (22.8%)
disease
The factory underwent corrective measures as well as repeated
sampling, and the foodstuff was recalled, shortly before the occur-
Blood stream 36 (67.9%) 22 (84.6%) 58 (73.4%) rence of the cluster. This pulsotype was also found in unrelated
infection
routine samples of cakes (in 2010 and 2013).
Other (arthritis or 3 (5.7%) – 3 (3.8%) Clusters 4 and 6 consisted of non-pregnancy-associated cases.
peritonitis) Cluster 4 included three tenants of the same nursing home
who fell ill a few days apart. They exclusively ate food that was
served at the nursing home, which was sampled by the District
Food Service as part of the epidemiological investigation.
Trace-back and molecular epidemiology
L. monocytogenes was isolated from cooked ground chicken
During the studied period, a total of 35 molecular clusters were which was served at the nursing home but it was not identical
identified in the Tel Aviv District. Six molecular and epidemiolo- to the bacteria that were isolated from the patients. The three
gic clusters are described for the purpose of this study, entailing patients died as a result of the illness. The additional case reported
38 patients (Table 4; Fig. 5). Smaller clusters of identical molecu- having eaten various packaged condiments, which were sampled
lar clones were found but were not described as we could not find but were not found to be contaminated with L. monocytogenes.
an epidemiologic link between the patients. This pulsotype has also been found in unrelated isolates of
Cluster 1 consisted of two newborns infected with the same ready-to-eat salads since 2008.
clone of L. monocytogenes. The two newborns were born on the The pulsotypes demonstrated in clusters 3 and 4 have been
same day in the same hospital and assisted by the same midwife. among the most commonly isolated genotypes in Israel, ever
The first newborn to develop symptoms was born to a mother since 2006.
that developed fever during pregnancy and delivered at 36 In cluster 6, epidemiologic inquiries were carried out for eight
weeks gestational age (GA). The mother was given antibiotics out of nine cases. Four patients reported having eaten cured or
during delivery and her cultures were negative for L. monocyto- smoked fish. One sample of smoked salmon taken by the
genes. The newborn had BSI, improved with antibiotic treatment District Food Service in a restaurant as part of the investigation
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https://doi.org/10.1017/S0950268817003004Epidemiology and Infection 287
Table 2. Clinical and bacterial serotype characteristics of non-pregnancy-associated cases, Tel Aviv District, Israel, 2010–2015
Non-pregnancy-associated
NID (%) BSI (%) Other (%) P value
Total 18 58 3
Median age in years (range) 66 (4–94) 77 (33–100) 79 (78–91) 0.29
Gender 0.272
Male 10 (56%) 20 (34%) 1 (33%)
Female 8 (44%) 38 (66%) 2 (67%)
Number of deaths 4 (22%) 22 (38%) – 0.101
Mean duration of hospitalisation (days) 15.4 11.5 24.5 0.028
Serotype 0.316
4b 7 (39%) 20 (34%) –
1/2a 4 (22%) 16 (28%) 1 (33%)
1/2b 1 (6%) 14 (24%) 1 (33%)
Unknown 6 (33%) 8 (14%) 1 (33%)
Table 3. Pregnancy-associated listeriosis outcome characteristics, Tel Aviv District, Israel, 2010–2015
Normal ongoing pregnancy Pre-term birth Miscarriage Neonatal listeriosis P value
Pregnant women (17) 5 5 7 – –
Newborns (6) – – – 6 –
Trimester of pregnancy 0.012
First trimester 1 – 1 –
Second trimester 3 – 5 –
Third trimester 1 5 1 6
Serotype 0.1
4b 3 4 5 5
1/2b 2 – 1 –
Unknown – 1 1 1
Fig. 4. Listeria monocytogenes serotypes isolated from
patients during the years, Tel Aviv District, Israel,
2010–2015.
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https://doi.org/10.1017/S0950268817003004288 M. Salama et al.
was positive for the L. monocytogenes of the same pulsotype. In
salads and sandwiches
addition, the same pulsotype was also found in other various
Food isolates (national)
Smoked and cured fish
smoked and cured fish across the country. All the factories
Various ready-to-eat
Raw fish in a sushi
which provided the contaminated foodstuffs recalled their fish
Cakes, deli meats
products, underwent sanitary investigations and were required
restaurant
to provide repeated food sampling to prove the end of the
L. monocytogenes contamination.
None
None
Discussion
This study describes the epidemiology and molecular findings of
Deaths
0
2
2
2
1
5
listeriosis patients in the Tel Aviv District during the 6-year per-
iod from 2010 to 2015.
We found an average rate of 1.3 per 100 000 population, which
2010 (1), 2012 (2), 2013 (3), 2014 (1)
is considerably higher than the reported EU average of 0.6 per
100 000 population [10]. Those high rates concur with previous
findings [6, 7] and can be attributed to a number of factors.
2012 (1), 2014 (2), 2015 (5)
The Tel Aviv District has the highest proportion of elderly popu-
Year (number of cases)
lation in Israel, with 15% being older than 65 years old [11] com-
pared with the national median of 11%. However, this can only
2010 (2), 2013 (1)
2011 (3), 2015 (1)
2014 (5), 2015 (4)
partly explain the high disease rates as age-specific listeriosis
rates were still higher in the Tel Aviv District compared to overall
national rates. Furthermore, the Tel Aviv District’s socio-
2013 (2)
economic level is one of the highest in Israel and enables better
access to medical care, with perhaps higher diagnosis rates.
The Tel Aviv District is a metropolitan district, which attracts
over 1 million tourists yearly. It has a high supply, and a high
Number of pregnancy-
demand, of restaurants and food markets, as well as a high con-
sumption of ready-to-eat foods, which are often imported. The
associated cases
restaurant turnover is particularly high, with a needed adaptation
2
1
1
0
6
0
time to learn basic hygienic measures, which hinders the proper
handling of food. We found that disease peaked during two
major holidays in which it is customary to consume meat and
Table 4. Selected clusters of clonal Listeria monocytogenes in the Tel Aviv District, Israel, 2010–2015
fish. Further study is needed to establish if this trend is consistent
and if so, periodic recommendations to thoroughly cook fish and
meat as well as for the handling of raw food to avoid cross-
Number of
contamination should be published.
2
3
7
4
8
9
cases
In our study, 23% of cases were pregnancy-associated.
Although the Tel Aviv District does not have a higher birth rate
compared with other districts [12], it has been previously
shown that it has the highest proportion of pregnancy-associated
Serotype
1/2a
cases compared with other districts [7]. Pregnant women often
4b
4b
4b
4b
4b
reported having eaten foods at higher risk for listeria contamin-
ation such as deli meats, pre-packed condiments or cured fish
[13, 14], which have been repeatedly recalled in Israel due to
GX6A12.0061.ISR
GX6A12.0025.ISR
GX6A12.0002.ISR
GX6A12.0002.ISR
GX6A12.0033.ISR
GX6A12.0001.ISR
L. monocytogenes contamination [15], but we were often left
with no laboratory evidence for the suspected exposure. Further
ApaI name
study is needed to elucidate the sources of infection in this par-
ticular category, as few women seem to be changing their eating
habits during pregnancy, and more targeted prevention methods
should be issued, notably through the attending physician.
In terms of molecular findings, the L. monocytogenes serotype
GX6A16.0024.ISR
GX6A16.0160.ISR
GX6A16.0003.ISR
GX6A16.0041.ISR
GX6A16.0001.ISR
GX6A16.0016.ISR
distribution was stable during the studied period, with 4b being
AscI name
the most widely distributed among clinical isolates. The pulso-
types were very diverse and the high rates of disease could not
be attributed to a specific strain. We identified a case of possible
nosocomial infection, in a nursery, suggesting contamination by a
healthcare worker. This is a rare but known form of L. monocyto-
genes transmission [16–18]. Such cases emphasise once again
number
Cluster
the importance of hand hygiene and maintaining a therapeutic
environment that is as sterile as possible. Another interesting
1
2
3
4
5
6
find was the positive food samples taken during the epidemiologic
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https://doi.org/10.1017/S0950268817003004Epidemiology and Infection 289
Fig. 5. Molecular clusters of Listeria monocytogenes isolates in the Tel Aviv District, Israel, 2010–2015.
investigations. Unfortunately, even after finding a L. monocyto- for practitioners, should be applied to increase awareness and pre-
genes isolate in the food sample with a corresponding serotype vention among susceptible populations, as the bacteria are
to the case (cluster 4, Table 4), the isolate was not genetically widespread and disease burden is heavy.
identical to the human isolates, accentuating the difficulty of find- As many countries are reporting increasing listeriosis rates
ing the food source. [19], partly explained by longer life spans, changing food-
In our study, dissimilar PFGE profiles were more informative handling methods and global exposure to foods from all over
than identical ones, as they were able to exclude suspicious food the world, enhanced and sustained routine sampling and molecu-
sources or common exposures. Identical profiles could only be lar analysis of foodstuffs, as well as surfaces in food factories and
informative if a link could be found in the epidemiologic inquiry. restaurants, should be implemented, as it is the most helpful tool
In those cases, whole-genome sequencing of the isolates could during epidemiologic investigations to unravel the source
potentially elucidate the occurrence of indistinguishable but not exposures.
epidemiologically linked PFGE clusters. We are implementing
this state of the art, high-resolution standardised method for all
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